this PDF file Anthropogenic Sources of NonMigratory Avian Mortalities In Singapore | TAN | The International Journal of Tropical Veterinary and Biomedical Research 1 PB
Open Acces
Int. J. Trop. Vet. Biomed. Res.
Vol. 2 (2) : 17-27; November 2017
www.jurnal.unsyiah.ac.id/IJTVBR
E-ISSN : 2503-4715
Anthropogenic Sources of Non-Migratory Avian Mortalities In Singapore
David J. X. TAN1,Ding Li YONG2,3,4, Bing Wen LOW2,4, Alan OWYONG4 and Alfred
CHIA4
1
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapor e
117543
2
South-east Asian Biodiversity Society, 504 Choa Chu Kang Street 51, #01-173, Singapore 680504
3
BirdLife International Asia, 354 Tanglin Road, #01-16/17, Tanglin International Centre, Singapore
247672
4
Nature Society (Singapore), 510 Geylang Road, #02-05, The Sunflower, Singapore 389466
Email for correspondence: david.tanjx@gmail.com
Abstract
Although urban spaces are increasingly recognised as viable habitats for wildlife, cities remain a major
source of anthropogenic mortality for wild birds. While the sources of urban avian mortalities have been well
documented in North America, these phenomena remain poorly studied in Southeast Asia, especially for resident
species. Here we present the first summary of non-migratory urban bird mortalities for the heavily urbanised island
of Singapore. We conducted a citizen science study using print and social media outreach to encourage members of
the public to report their observations of dead birds between November 2013 and October 2017, and collected a total
of 362 mortality records across 65 resident bird species and five mortality sources. Our results show that a diverse
array of bird species is directly impacted by anthropogenic sources of mortality, although mortalities stemming from
roadkill and cat predation are likely to be undersampled. We also find that forest-edge frugivores such as the Pinknecked Green Pigeon are likely to be especially vulnerable to building collisions. Our study shows that despite its
limitations, opportunistic sampling using citizen science can generate large amounts of ecological data at relatively
low cost, and serve as a cost-effective complement to standardised survey methodologies.
Key words : bird mortality, building collisions, urban ecology, cats, human impacts, roadkill, citizen science
Background
Cities present a considerable array of
impediments to the movement of wildlife.
The proliferation of densely built-up areas
with high volumes of vehicular traffic, as
well as the introduction of domesticated
predators such as cats, all contribute to the
anthropogenic mortalities of wildlife in
urban areas (Loss et al., 2015).
Birds in particular are especially
susceptible to urban mortality resulting from
anthropogenic factors. Studies stemming
primarily from North America have shown
that cat predation (Lepczyk et al., 2004;
Loss et al., 2013), building collisions (Klem,
2015, 1989), and roadkill (Kociolek et al.,
2011), account for a significant proportion
of observed urban avian mortalities (Loss et
al., 2015). In the United States, for instance,
it is estimated that between 365 and 988
million birds die from collisions with
buildings annually, while another 1.31 to
3.99 billion birds die as a result of predation
by cats every year (Loss et al., 2014), with
similar mortality trends observed in Canada
(Calvert et al., 2013) and Australia
(Woinarski et al., 2017). With city
biodiversity receiving increased focus as
part of broader biodiversity conservation
strategies (Chan et al., 2014), understanding
the sources and impacts of anthropogenic
mortality in birds is essential to mitigating
and ultimately reducing the deleterious
impacts of cities on wild bird populations.
While the anthropogenic sources of
avian mortality have been relatively well
documented in temperate zones, these
phenomena have largely been overlooked in
the tropics, especially in Southeast Asia.
Aside from a single study from Singapore
describing the patterns of migratory
mortalities resulting from building collisions
17
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
(Low et al., 2017), there exists little other
available data in the scientific literature
about the sources of urban avian mortalities
in Southeast Asia despite the region having
one of the fastest growing urban populations
in the world (United Nations, Department of
Economic and Social Affairs, 2015).
In this study, we summarise the
results of a multi-year citizen science survey
of avian mortalities across the heavily
urbanised island nation of Singapore, with a
specific focus on the anthropogenic sources
of mortality of resident species. We compare
the results of our survey with the migratory
mortality data reported in Low et al. (2017)
as well as with other comparable studies to
determine if the pattern of urban avian
mortalities in Singapore is congruent with
patterns observed in other parts of the world,
and highlight the challenges and limitations
inherent in assessing the impacts of cities on
bird populations.
Materials and Methods
Study Area
We conducted the study in Singapore
(1.150°-1.483°N and 103.633°-104.100°E),
a 719.2 sq. km island south of Peninsular
Malaysia, located within the Sundaland
biodiversity hotspot in Southeast Asia.
Singapore is one of the most heavily
urbanised and densely populated nations in
the world, with 100% of its population
residing in urban areas (United Nations,
Department of Economic and Social Affairs,
2015) comprising approximately 52% of its
total landmass (Tan, 2015). Despite this,
Singapore continues to maintain substantial
patches of urban greenery and forest
vegetation, with managed vegetation
covering approximately 16% of Singapore’s
total land area (Tan, 2015), and
approximately 0.16% and 20% of
Singapore’s landmass comprised of primary
and secondary forest vegetation respectively
(Yee et al., 2011). The combination of highdensity urban development and extensive
greenery in close proximity to urban areas
has resulted in urban Singapore having a
relatively high diversity of avian species,
both resident and migratory (Lim, 2009).
18
Mortality Documentation
We documented urban avian mortality
records from across Singapore between
November 2013 and October 2017 via a
rudimentary citizen science protocol.
Members of the public were encouraged via
print media (Feng, 2013) and social media
platforms such as FaceBook and Instagram
to submit observations of dead or injured
birds. All record submissions were verified
and identified to species based on
photographic documentation or, where
possible, collected specimens. Additionally,
we collected as much information as
possible on the locality, age, and likely
cause of death of each record. Birds found at
the base of buildings and exhibiting any
form of facial injury or head trauma were
listed as having died of building collisions,
while birds found on or by the sides of roads
with injuries indicative of blunt force trauma
were identified as roadkill. Identifying
instances of cat predation was considerably
more challenging, and only specimens that
were directly observed being killed by cats
and/or self-reported by cat owners were
included in our records. All other instances
of predation for which the predator was
unknown had the likely cause of death listed
simply as ‘predation’. Specimens for which
the cause of death was known but
attributable to freak accidents (e.g. falling
out of the nest) had their likely cause of
death listed as ‘misadventure’. Absent better
methods for assessing cause of death, all
other bird mortality records had their cause
of death listed as ‘unknown’. We discounted
the existence of mortalities resulting from
power line, communications tower, or wind
farm collisions as such aboveground
obstacles are generally absent in Singapore.
For the purposes of this study, we
reported records belonging only to resident
and naturalised species, and excluded all
migratory and escapee species.
Outlier Analysis
To test for potential outlier species
that may be overrepresented in the mortality
dataset, we conducted a simple linear
regression analysis to compare the
population densities of the 10 most abundant
resident bird species in urban Singapore (per
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Tan 2016) with the number of urban
mortality records.
Spatial Distribution of Resident and
Migratory Building Collision Mortalities
To compare the spatial distribution
of resident and migratory building collision
mortalities, we filtered our dataset to
exclude records without complete GPS
coordinates and separately plotted resident
and migratory building collision mortality
records on a map of Singapore using QGIS
v2.18.9 (QGIS Development Team 2016).
For both the resident and migratory datasets,
we subsequently used the heatmap v0.2
plugin with a radius parameter set at 1,000
m and the QGIS raster calculator to identify
hotspots with a pixel value greater than two,
and overlaid the resident and migratory
collision hotspot polygons on a single map
canvas.
Results
Summary of Mortality Records
We documented a total of 362 mortality
records from 65 species during the surveyed
period, of which 104 mortalities were the
result of building collisions, 16 from
vehicular collisions, 10 due to predation – of
which 7 were attributable to cats – and 7
records resulting from misadventure (Table
1). 225 records had an unknown cause of
death, often due to specimens having been
moved post-mortem or specimens in
advanced stages of decay (Table 1). 21% (n
= 76) of the records were identified as
juveniles, with 24 building collision cases, 1
roadkill case, 1 instance of cat predation, 4
cases of misadventure, and 46 individuals
with an unknown cause of death (Table 1).
Pigeons (family Columbidae) formed
the largest proportion (32.6%) of the
mortality records, with 73 Pink-necked
Green Pigeon (Treron vernans) records
comprising 61.9% of the total pigeon
mortalities. Of the pigeon records with a
known cause of death, 88.9% were the result
of building collisions, which suggests that
pigeons may be especially susceptible to
collisions with urban structures.
Starlings and mynas (family
Sturnidae) were the second-largest taxon
amongst the reported urban mortalities
(22.1%), with most of the mortalities in this
family comprised of Asian Glossy Starlings
(Aplonis panayensis) and Javan Mynas
(Acridotheres javanicus). Interestingly,
juveniles formed 81% of the total Asian
Glossy Starling building collision records
(Fig. 1).
Plotting
the
distribution
of
mortalities over time, we find that juvenile
mortalities peak during the months of May
and June, and again in October and
November (Fig. 1). As for overall
mortalities, we observe a relative decrease in
the number of mortality records between the
months of May and September (Fig. 1).
Testing for Outliers
Correlating population densities with
number of mortalities for the 10 most
abundant species in Singapore, we find a
general positive linear correlation between
population density and number of
mortalities, with the exception of the Pinknecked Green Pigeons and Asian Glossy
Starlings, which exhibit far higher mortality
rates than would be expected based on their
population density (Fig. 2).
Comparing Resident and Migratory
Building Collisions
Plotting the spatial distribution of building
collision victims, we find two broad regions
where resident and migratory collision
hotspots overlap (Fig. 3), both of which are
located in the central region of Singapore
(see Low et al. (2017) for regional
delimitation of Singapore island), with one
hotspot occurring around the National
University of Singapore campus (Region A,
Fig. 3) and the other occurring over the
Heritage and Central Business Districts
(Region B, Fig. 3). We also observed an
absence of collision hotspots for resident
species in the western region of Singapore,
in contrast to the high number of migratory
building collisions in that region (Fig. 3;
Low et al. 2017).
Discussion
Our study documents for the first
time the wide array of non-migratory
Southeast Asian bird species affected by
anthropogenic sources of mortality, with
19
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
species representing all but one order
(podicipediformes) of resident avians known
for Singapore. However, it should be noted
that
our
opportunistic
sampling
methodology might result in artifacts that
may bias the data. Here we discuss the
implications of our data and the caveats that
need to be taken into account when
interpreting
our
dataset
for
each
anthropogenic mortality source.
Building Collisions
Our results show that while 32 nonmigratory species are affected by building
collisions (Table 1), some species are likely
more susceptible than others. In particular,
Pink-necked Green Pigeons and juvenile
Asian Glossy Starlings, and to a lesser
extent
the
Asian
Emerald
Doves
(Chalcophaps indica ), appear to be
overrepresented in the building collision
dataset (Table 1), and in the case of the
Pink-necked Green Pigeon and Asian
Glossy Starling, exhibit higher mortality
rates than their estimated population
densities would suggest (Fig. 2). The fact
that all three ‘super collider’ species are
forest-edge frugivores suggests that both
feeding guild and local dispersal behaviour
may affect a species’ susceptibility to
collision. Given the patchy distribution of
parks and forest fragments in Singapore
(Castelletta et al., 2005), it is likely that
these nomadic forest edge frugivores pass
through urban areas as part of their foraging
movements, which increases the likelihood
of building collisions occurring. Brisque et
al. (2017) have also found in Brazil that
Columbids appear to be more prone to
window collisions, which may explain why
all resident pigeon species in Singapore save
for the Rock Pigeon (Columba livia ) and the
extremely rare Little Green Pigeon (Treron
olax) are represented in our building
collision dataset (Lim, 2009). In addition,
the observation that juveniles form the
majority of Asian Glossy Starling building
collision mortalities suggests that collision
avoidance may be a learnt behaviour in this
species (Klem, 2014). It should be noted,
however, that sampling bias might also
contribute to the relatively high proportion
of Pink-necked Green Pigeon, Asian Glossy
20
Starling, and Asian Emerald Dove mortality
records. The large size and colourful
plumage of both pigeon species, as well as
the propensity for entire flocks of Asian
Glossy Starlings to collide with buildings at
the same time, result in these species being
highly conspicuous and detectable to casual
observers, and increases their likelihood of
being reported relative to other species
within
an
opportunistic
sampling
framework.
Comparing the number of resident
and migratory building collisions, our
results show that for the same sampling
period and the same sampling methodology,
we observe twice as many migratory
mortalities (n = 204) as resident mortalities
(n = 104; Table 1). This is consistent with
findings from both the neotropics and
nearctic, which show that migratory species
are more vulnerable to building collisions
than year-round residents (Agudelo-Álvarez
et al., 2010; Arnold and Zink, 2011; Kahle
et al., 2016).
As for the spatial distribution of
migratory and resident building collision
mortalities, while it is tempting to
overanalyse the results of the spatial
analysis, it should be noted that hotspots are
likely to be highly biased by uneven
sampling effort. The existence of
overlapping migratory and resident hotspots
over the National University of Singapore
(Region A, Fig. 3), for instance, is likely due
to a higher observer density relative to the
rest of Singapore. Regardless, the existence
of overlapping resident and migratory
hotspots in the Heritage and Central
Business District (Region B; Fig. 3) as well
as non-overlapping resident and migratory
hotspots in the central and western regions
of Singapore indicate that there are likely
both common and unique urban abiotic
factors affecting the likelihood of resident
and migratory building collision mortalities.
Roadkill and Cat Predation
In contrast to the building collision
mortalities, we observed far fewer roadkill
and cat predation mortalities in our dataset,
with twice as many roadkill mortalities as
cat predation mortalities (Table 1). The
results of our study appear to be incongruent
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
with the conclusions of Loss et al. (2013)
and Calvert et al. (2013), who find that cats
are responsible for the highest number of
avian mortalities in the United States and in
Canada respectively. This inconsistency
suggests that we have likely undersampled
the true extent of cat-based mortalities in our
study.
Temporal
variation
in
resident
mortalities
While the temporal pattern of
juvenile mortalities corresponds generally
with known breeding cycles in Singapore,
the observed dip in non-juvenile mortalities
in the middle of the year, with a slight
decline between May and June, and a larger
decline between July and September, does
not seem consistent with expectations since
adult mortality rates should remain
relatively stable throughout the year (Fig. 1).
The correlation of the non-juvenile mortality
peaks with the migratory months (October
to April) suggests that the mid-year dip
might
be
due
to
observational
autocorrelation, where observers are less
observant when overall mortalities are low
and vice versa, although this will need to be
ascertained using more structured sampling
methods.
Challenges and opportunities of citizen
science
The numerous caveats we have raised here
highlight the challenges of combining
opportunistic sampling with citizen science.
The uneven sampling of localities, varying
detectabilities of different species, and the
impacts of sampling autocorrelation and
sampling fatigue result in data that is often
inconsistent
and
incomplete,
which
confounds efforts at drawing rigorous
quantitative insights from the data. Despite
this, the results of our study show that
citizen science provides a cost-effective
means of gathering large amounts of data on
a diffuse and stochastic phenomenon, with
the added benefit of simultaneously
engaging in public outreach and education.
Our results therefore show that citizen
science can function as a cheap and effective
complement to more standardised survey
methodologies (Dickinson et al., 2010),
especially in intensively developed urban
areas such as Singapore.
Tables and Figures
Table 1: Summary of urban avian mortality records for Singapore, with families ordered per
Jarvis et al. (2014) and names following Eaton et al. (2016). Cause of death abbreviations are as
follows: BC, building collisions; RK, roadkill; CA, cat predation; PR, predation by unknown
predator; MA, misadventure; UK, unknown. Numbers in parentheses are numbers of juvenile
and fledgling mortalities.
Family
Anatidae
Species
Lesser Whistling-duck (Dendrocygna
Cause of Death
Total
BC
RK
CA
PR
MA
UK
-
-
-
-
-
1
1
javanica )
Phasianidae
Red Junglefowl (Gallus gallus)
1
1
-
-
-
2
4
Columbidae
Asian Emerald Dove (Chalcophaps
11
-
-
-
-
5
16
Rock Pigeon (Columba livia )
-
-
-
-
-
7
7
Pied Imperial Pigeon (Ducula bicolor )
2
1
-
-
-
1
4
Zebra Dove (Geopelia striata )
1
-
-
-
-
2
3
indica )
(1)
Spotted Dove (Spilopelia chinensis)
1
2
-
-
1
9
13
Pink-necked Green Pigeon (Treron
32
-
1
1
-
39
73
vernans)
(4)
(5)
21
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Thick-billed Green Pigeon (Treron
1
-
-
-
-
1
2
1
-
-
-
-
-
1
1
-
-
-
-
2
3
3
1
-
-
-
7
11
curvirostra )
Cuculidae
Banded Bay Cuckoo (Cacomantis
sonneratii)
Little Bronze Cuckoo (Chrysococcyx
minutillus)
Asian Koel (Eudynamys scolopaceus )
(1)
Caprimulgidae
(1)
Savanna Nightjar (Caprimulgus affinis )
-
-
-
-
-
1
1
Large-tailed Nightjar (Caprimulgus
-
-
-
-
-
4
4
1
-
-
-
-
3
4
Plume-toed Swiftlet (Colocalia affinis)
-
-
-
-
-
1
1
Grey-rumped Treeswift (Hemiprocne
-
-
-
-
-
1
1
-
4
1
-
-
3
8
Red-legged Crake (Rallina fasciata )
-
1
-
-
-
3
4
Slaty-breasted Rail (Lewinia striata )
-
-
-
-
-
3
3
Lapwing (Vanellus sp.)
-
-
-
-
-
1
1
macrurus)
Apodidae
Edible-nest Swiftlet (Aerodramus
fuciphagus)
Hemiprocnidae
longipennis)
Rallidae
White-breasted Waterhen (Amaurornis
phoenicurus)
Charadriidae
(1)
Ardeidae
Purple Heron (Ardea purpurea )
-
-
-
-
1
-
1
(1)
Accipitridae
Cattle Egret (Ardea ibis)
-
-
-
-
-
1
1
Striated Heron (Butorides striata )
-
-
-
-
-
3
3
Crested Goshawk (Lophospiza
2 (1)
-
-
-
-
2
4
trivirgata )
White-bellied Fish-eagle (Ichthyophaga
(1)
1
-
-
-
-
-
1
Brahminy Kite (Haliastur indus)
-
-
-
-
-
1
1
Changeable Hawk-Eagle (Nisaetus
2 (1)
-
-
-
-
-
2
Crested Serpent Eagle (Spilornis cheela )
1
-
-
-
-
-
1
Collared Scops Owl (Otus lempiji)
-
1
-
-
-
1
2
Spotted Wood Owl (Strix seloputo )
-
-
-
-
-
1
1
Barn Owl (Tyto alba )
1
-
-
-
-
3
4
Oriental Pied Hornbill (Anthracoceros
-
-
-
-
-
1
1
leucogaster )
limnaeetus)
Strigidae
Bucerotidae
albirostris)
Megalaimidae
Coppersmith Barbet (Psilopogon
(1)
1
-
-
-
-
3
4
Lineated Barbet (Psilopogon lineatus)
1
-
-
-
-
-
1
Sunda Pygmy-woodpecker (Picoides
-
-
-
-
-
1
1
haemacephalus)
Picidae
moluccensis)
22
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Common Flameback (Dinopium
-
-
-
-
javanense)
Alcedinidae
White-breasted Kingfisher (Halcyon
1
1
3
4
(1)
1
-
-
-
-
smyrnensis)
Collared Kingfisher (Todiramphus
-
(1)
1
-
-
-
-
2
3
-
-
-
-
-
1
1
chloris)
Coraciidae
Common Dollarbird (Eurystomus
orientalis)
Psittacidae
Blue-crowned Hanging Parrot (Loriculus
(1)
1
-
-
-
-
1
2
1
-
-
-
-
1
2
1
-
-
-
-
1
2
galgulus)
Red-breasted Parakeet (Psittacula
alexandri)
Long-tailed Parakeet (Psittacula
longicauda )
(1)
Aegithinidae
Common Iora (Aegithina tiphia )
-
-
-
-
-
2
2
Cisticolidae
Ashy Tailorbird (Orthotomus ruficeps )
-
-
-
-
-
1
1
Common Tailorbird (Orthotomus
-
-
-
-
1
-
1
sutorius)
Dicaedae
Scarlet-backed Flowerpecker (Dicaeum
(1)
3 (1)
-
-
-
-
2
5
-
-
-
1
-
1
2
White-headed Munia (Lonchura maja )
1
-
-
-
-
-
1
Scaly-breasted Munia (Lonchura
2
-
-
-
-
5
7
Javan Munia (Lonchura leucogastroides )
-
-
-
-
-
1
1
Irenidae
Asian Fairy Bluebird (Irena puella )
-
-
-
-
-
1
1
Muscicapidae
Oriental Magpie-robin (Copsychus
1
-
1
-
-
3
5
cruentatum)
Dicruridae
Greater Racket-tailed Drongo (Dicrurus
paradiseus)
Estrildidae
punctulata )
saularis)
Nectariniidae
Brown-throated Sunbird (Anthreptes
(2)
-
-
-
-
-
malacensis)
Ornate Sunbird (Cinnyris ornatus)
1
(1)
-
-
1
-
-
(1)
Little Spiderhunter (Arachnothera
1
3
4
(1)
-
-
-
-
-
1
1
-
2
1
-
1
6
10
(1)
(4)
-
2
longirostra )
Oriolidae
Passeridae
Black-naped Oriole (Oriolus chinensis)
Eurasian Tree Sparrow (Passer
2
-
1
-
montanus)
Pycnonotidae
Sunda Yellow-vented Bulbul
(1)
-
-
-
-
-
(Pycnonotus analis)
Olive-winged Bulbul (Pyccnonotus
5
16
16
(5)
2
-
-
-
-
1
3
2
3
-
1
2
22
30
plumosus)
Sturnidae
Javan Myna (Actidotheres javanicus)
23
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
(5)
Zosteropidae
Common Myna (Acridotheres tristis)
-
-
-
-
-
1
1
Asian Glossy Starling (Aplonis
21
-
-
-
-
26
47
panayensis)
(17)
Common Hill Myna (Gracula religiosa )
-
-
-
-
-
2
2
Sunda White-eye (Zosterops melanurus)
1
-
1
-
-
6
8
(13)
(1)
Total
104
16
7
3
7
225
362
Figure 1: Reported resident mortalities by month, stratified by age category. The two peaks in
juvenile and fledgling mortalities in May and November likely correspond with primary and
secondary breeding periods (Lim, 2009). It is unclear why there exists a dip in mortality records
during the months of July to September.
Correla on between avian popula on density and number
of mortali es for the 10 most abundant bird species
80
Pink-necked Green
Pigeon
70
Numner of Mortali es
60
50
Asian Glossy Starling
40
y = 14.649x
R² = -0.5047
30
20
10
0
0
0.5
1
1.5
2
2.5
3
Popula on Density (ha-1)
Figure 2: Correlation between avian population density (derived from Tan (2016)) and number
of mortalities for the 10 most abundant species in Singapore. The scatterplot shows a general
positive linear correlation between population density and number of recorded mortalities, with
24
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
the notable exception of the Pink-necked Green Pigeon and the Asian Glossy Starling, which
suggests that these two species may either be more susceptible to urban mortalities or subject to
positive sampling bias.
Figure 3: Spatial distribution of resident and migratory building collisions in Singapore, with
shaded regions highlighting likely collision hotspots. Overlaying the inferred collision hotspots
of both resident and migratory species shows two regions of overlap, with one region centering
around the National University of Singapore campus (region A) and the other around the
Heritage and Central Business Districts (region B)
Mortality in Canada. Avian Conserv.
Ecol.
8,
11.
References
Agudelo-Álvarez, L., Moreno-Velasquez, J.,
https://doi.org/http://dx.doi.org/10.5751
Ocampo-Peñuela, N., 2010. Colisiones
/ACE-00581-080211
de aves contra ventanales en un campus
Castelletta, M., Thiollay, J.-M., Sodhi, N.S.,
universitario de bogotá, colombia.
2005. The effects of extreme forest
Ornitol. Colomb. 10, 3–10.
fragmentation on the bird community
Arnold, T.W., Zink, R.M., 2011. Collision
of Singapore Island. Biol. Conserv.
mortality has no discernible effect on
121,
135–155.
population trends of North American
https://doi.org/10.1016/j.biocon.2004.0
birds.
PLoS
One
6,
1–6.
3.033
https://doi.org/10.1371/journal.pone.00
Chan, L., Hillel, O., Elmqvist, T., Werner,
24708
P., Holman, N., Mader, A., Calcaterra,
Brisque, T., Campos-Silva, L.A., Piratelli,
E., 2014. USER ’ S MANUAL ON
A.J., 2017. Relationship between birdTHE SINGAPORE INDEX ON
of-prey decals and bird-window
CITIES ’ BIODIVERSITY ( also
collisions on a Brazilian university
known as the City Biodiversity Index ).
campus.
Zoologia
34,
1–8.
National Parks Board, Singapore,
https://doi.org/10.3897/zoologia.34.e13
Singapore.
729
Dickinson, J.L., Zuckerberg, B., Bonter,
Calvert, A.M., Bishop, C. a, Elliot, R.D.,
D.N., 2010. Citizen Science as an
Krebs, E. a, Kydd, T.M., Machtans,
Ecological Research Tool: Challenges
C.S., Robertson, G.J., 2013. A
and Benefits. Annu. Rev. Ecol. Evol.
Synthesis of Human-related Avian
Syst.
41,
149–172.
25
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
https://doi.org/10.1146/annurevecolsys-102209-144636
Eaton, J.A., van Balen, B., Brickle, N.W.,
Rheindt, F.E., 2016. Birds of the
Indonesian
Archipelago:
Greater
Sundas and Wallacea, First. ed. Lynx
Edicions, Barcelona.
Feng, Z., 2013. Team flocks to collect dead
birds for research. The Straits Times.
Jarvis, E.D., Mirarab, S., Aberer, A.J., Li,
B., Houde, P., Li, C., Ho, S.Y.W.,
Faircloth, B.C., Nabholz, B., Howard,
J.T., Suh, A., Weber, C.C., da Fonseca,
R.R., Li, J., Zhang, F., Li, H., Zhou, L.,
Narula, N., Liu, L., Ganapathy, G.,
Boussau,
B.,
Bayzid,
M.S.,
Zavidovych, V., Subramanian, S.,
Gabaldon, T., Capella-Gutierrez, S.,
Huerta-Cepas, J., Rekepalli, B., Munch,
K., Schierup, M., Lindow, B., Warren,
W.C., Ray, D., Green, R.E., Bruford,
M.W., Zhan, X., Dixon, A., Li, S., Li,
N., Huang, Y., Derryberry, E.P.,
Bertelsen, M.F., Sheldon, F.H.,
Brumfield, R.T., Mello, C. V., Lovell,
P. V., Wirthlin, M., Schneider, M.P.C.,
Prosdocimi, F., Samaniego, J.A.,
Velazquez, A.M. V., Alfaro-Nunez, A.,
Campos, P.F., Petersen, B., SicheritzPonten, T., Pas, A., Bailey, T.,
Scofield, P., Bunce, M., Lambert,
D.M., Zhou, Q., Perelman, P., Driskell,
A.C., Shapiro, B., Xiong, Z., Zeng, Y.,
Liu, S., Li, Z., Liu, B., Wu, K., Xiao,
J., Yinqi, X., Zheng, Q., Zhang, Y.,
Yang, H., Wang, J., Smeds, L.,
Rheindt, F.E., Braun, M., Fjeldsa, J.,
Orlando, L., Barker, F.K., Jonsson,
K.A., Johnson, W., Koepfli, K.-P.,
O’Brien, S., Haussler, D., Ryder, O.A.,
Rahbek, C., Willerslev, E., Graves,
G.R., Glenn, T.C., McCormack, J.,
Burt, D., Ellegren, H., Alstrom, P.,
Edwards, S. V., Stamatakis, A.,
Mindell, D.P., Cracraft, J., Braun, E.L.,
Warnow, T., Jun, W., Gilbert, M.T.P.,
Zhang, G., 2014. Whole-genome
analyses resolve early branches in the
tree of life of modern birds. Science
(80-.
).
346,
1320–1331.
https://doi.org/10.1126/science.125345
1
Kahle, L.Q., Flannery, M.E., Dumbacher,
26
J.P., 2016. Bird-Window Collisions at a
West-Coast Urban Park Museum:
Analyses of Bird Biology and Window
Attributes from Golden Gate Park, San
Francisco. PLoS One 11, e0144600.
https://doi.org/10.1371/journal.pone.01
44600
Klem, D., 2015. Bird-Window Collisions: A
Critical
Animal
Welfare
and
Conservation Issue. Appl. Anim. Welf.
Sci.
18,
S11–S17.
https://doi.org/10.1080/10888705.2015.
1075832
Klem, D., 2014. Landscape, Legal, and
Biodiversity Threats that Windows
Pose to Birds: A Review of an
Important Conservation Issue. Land 3,
351–361.
https://doi.org/10.3390/land3010351
Klem, D., 1989. Bird-window collisions.
Wilson Bull. 4, 606–620.
Kociolek, A. V., Clevenger, A.P., St. Clair,
C.C., Proppe, D.S., 2011. Effects of
Road Networks on Bird Populations.
Conserv.
Biol.
25,
241–249.
https://doi.org/10.1111/j.15231739.2010.01635.x
Lepczyk, C.A., Mertig, A.G., Liu, J., 2004.
Landowners and cat predation across
rural-to-urban
landscapes.
Biol.
Conserv.
115,
191–201.
https://doi.org/10.1016/S00063207(03)00107-1
Lim, K.S., 2009. The Avifauna of
Singapore. Nature Society (Singapore),
Singapore.
Loss, S.R., Will, T., Loss, S.S., Marra, P.P.,
2014. Bird–building collisions in the
United States: Estimates of annual
mortality and species vulnerability.
Condor
116,
8–23.
https://doi.org/10.1650/CONDOR-13090.1
Loss, S.R., Will, T., Marra, P.P., 2015.
Direct Mortality of Birds from
Anthropogenic Causes. Annu. Rev.
Ecol. Evol. Syst. 46, 99–120.
https://doi.org/10.1146/annurevecolsys-112414-054133
Loss, S.R., Will, T., Marra, P.P., 2013. The
impact of free-ranging domestic cats on
wildlife of the United States. Nat.
Commun.
4,
1396.
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
https://doi.org/10.1038/ncomms2380
Low, B.W., Yong, D.L., Tan, D., Owyong,
A., Chia, A., 2017. Migratory bird
collisions with man-made structures in
South-East Asia : a case study from
Singapore. BirdingASIA 27, 107–111.
Tan, D.J.X., 2016. A quantitative survey of
avian population densities in a
heterogeneous
tropical
urban
landscape. Raffles Bull. Zool. 2016.
Tan, D.J.X., 2015. Population Dynamics of
the Striped Tit-Babbler in Singapore.
National University of Singapore.
United Nations, Department of Economic
and Social Affairs, P.D., 2015. World
urbanization prospects. United Nations,
New York.
Woinarski, J.C.Z., Murphy, B.P., Legge,
S.M., Garnett, S.T., Lawes, M.J.,
Comer, S., Dickman, C.R., Doherty,
T.S., Edwards, G., Nankivell, A.,
Paton, D., Palmer, R., Woolley, L.A.,
2017. How many birds are killed by
cats in Australia? Biol. Conserv. 214,
76–87.
https://doi.org/10.1016/j.biocon.2017.0
8.006
Yee, A.T.K., Corlett, R.T., Liew, S.C., Tan,
H.T.W., 2011. The vegetation of
Singapore ― an updated map. Gard.
Bull. Singapore 63, 205–212.
27
Int. J. Trop. Vet. Biomed. Res.
Vol. 2 (2) : 17-27; November 2017
www.jurnal.unsyiah.ac.id/IJTVBR
E-ISSN : 2503-4715
Anthropogenic Sources of Non-Migratory Avian Mortalities In Singapore
David J. X. TAN1,Ding Li YONG2,3,4, Bing Wen LOW2,4, Alan OWYONG4 and Alfred
CHIA4
1
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapor e
117543
2
South-east Asian Biodiversity Society, 504 Choa Chu Kang Street 51, #01-173, Singapore 680504
3
BirdLife International Asia, 354 Tanglin Road, #01-16/17, Tanglin International Centre, Singapore
247672
4
Nature Society (Singapore), 510 Geylang Road, #02-05, The Sunflower, Singapore 389466
Email for correspondence: david.tanjx@gmail.com
Abstract
Although urban spaces are increasingly recognised as viable habitats for wildlife, cities remain a major
source of anthropogenic mortality for wild birds. While the sources of urban avian mortalities have been well
documented in North America, these phenomena remain poorly studied in Southeast Asia, especially for resident
species. Here we present the first summary of non-migratory urban bird mortalities for the heavily urbanised island
of Singapore. We conducted a citizen science study using print and social media outreach to encourage members of
the public to report their observations of dead birds between November 2013 and October 2017, and collected a total
of 362 mortality records across 65 resident bird species and five mortality sources. Our results show that a diverse
array of bird species is directly impacted by anthropogenic sources of mortality, although mortalities stemming from
roadkill and cat predation are likely to be undersampled. We also find that forest-edge frugivores such as the Pinknecked Green Pigeon are likely to be especially vulnerable to building collisions. Our study shows that despite its
limitations, opportunistic sampling using citizen science can generate large amounts of ecological data at relatively
low cost, and serve as a cost-effective complement to standardised survey methodologies.
Key words : bird mortality, building collisions, urban ecology, cats, human impacts, roadkill, citizen science
Background
Cities present a considerable array of
impediments to the movement of wildlife.
The proliferation of densely built-up areas
with high volumes of vehicular traffic, as
well as the introduction of domesticated
predators such as cats, all contribute to the
anthropogenic mortalities of wildlife in
urban areas (Loss et al., 2015).
Birds in particular are especially
susceptible to urban mortality resulting from
anthropogenic factors. Studies stemming
primarily from North America have shown
that cat predation (Lepczyk et al., 2004;
Loss et al., 2013), building collisions (Klem,
2015, 1989), and roadkill (Kociolek et al.,
2011), account for a significant proportion
of observed urban avian mortalities (Loss et
al., 2015). In the United States, for instance,
it is estimated that between 365 and 988
million birds die from collisions with
buildings annually, while another 1.31 to
3.99 billion birds die as a result of predation
by cats every year (Loss et al., 2014), with
similar mortality trends observed in Canada
(Calvert et al., 2013) and Australia
(Woinarski et al., 2017). With city
biodiversity receiving increased focus as
part of broader biodiversity conservation
strategies (Chan et al., 2014), understanding
the sources and impacts of anthropogenic
mortality in birds is essential to mitigating
and ultimately reducing the deleterious
impacts of cities on wild bird populations.
While the anthropogenic sources of
avian mortality have been relatively well
documented in temperate zones, these
phenomena have largely been overlooked in
the tropics, especially in Southeast Asia.
Aside from a single study from Singapore
describing the patterns of migratory
mortalities resulting from building collisions
17
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
(Low et al., 2017), there exists little other
available data in the scientific literature
about the sources of urban avian mortalities
in Southeast Asia despite the region having
one of the fastest growing urban populations
in the world (United Nations, Department of
Economic and Social Affairs, 2015).
In this study, we summarise the
results of a multi-year citizen science survey
of avian mortalities across the heavily
urbanised island nation of Singapore, with a
specific focus on the anthropogenic sources
of mortality of resident species. We compare
the results of our survey with the migratory
mortality data reported in Low et al. (2017)
as well as with other comparable studies to
determine if the pattern of urban avian
mortalities in Singapore is congruent with
patterns observed in other parts of the world,
and highlight the challenges and limitations
inherent in assessing the impacts of cities on
bird populations.
Materials and Methods
Study Area
We conducted the study in Singapore
(1.150°-1.483°N and 103.633°-104.100°E),
a 719.2 sq. km island south of Peninsular
Malaysia, located within the Sundaland
biodiversity hotspot in Southeast Asia.
Singapore is one of the most heavily
urbanised and densely populated nations in
the world, with 100% of its population
residing in urban areas (United Nations,
Department of Economic and Social Affairs,
2015) comprising approximately 52% of its
total landmass (Tan, 2015). Despite this,
Singapore continues to maintain substantial
patches of urban greenery and forest
vegetation, with managed vegetation
covering approximately 16% of Singapore’s
total land area (Tan, 2015), and
approximately 0.16% and 20% of
Singapore’s landmass comprised of primary
and secondary forest vegetation respectively
(Yee et al., 2011). The combination of highdensity urban development and extensive
greenery in close proximity to urban areas
has resulted in urban Singapore having a
relatively high diversity of avian species,
both resident and migratory (Lim, 2009).
18
Mortality Documentation
We documented urban avian mortality
records from across Singapore between
November 2013 and October 2017 via a
rudimentary citizen science protocol.
Members of the public were encouraged via
print media (Feng, 2013) and social media
platforms such as FaceBook and Instagram
to submit observations of dead or injured
birds. All record submissions were verified
and identified to species based on
photographic documentation or, where
possible, collected specimens. Additionally,
we collected as much information as
possible on the locality, age, and likely
cause of death of each record. Birds found at
the base of buildings and exhibiting any
form of facial injury or head trauma were
listed as having died of building collisions,
while birds found on or by the sides of roads
with injuries indicative of blunt force trauma
were identified as roadkill. Identifying
instances of cat predation was considerably
more challenging, and only specimens that
were directly observed being killed by cats
and/or self-reported by cat owners were
included in our records. All other instances
of predation for which the predator was
unknown had the likely cause of death listed
simply as ‘predation’. Specimens for which
the cause of death was known but
attributable to freak accidents (e.g. falling
out of the nest) had their likely cause of
death listed as ‘misadventure’. Absent better
methods for assessing cause of death, all
other bird mortality records had their cause
of death listed as ‘unknown’. We discounted
the existence of mortalities resulting from
power line, communications tower, or wind
farm collisions as such aboveground
obstacles are generally absent in Singapore.
For the purposes of this study, we
reported records belonging only to resident
and naturalised species, and excluded all
migratory and escapee species.
Outlier Analysis
To test for potential outlier species
that may be overrepresented in the mortality
dataset, we conducted a simple linear
regression analysis to compare the
population densities of the 10 most abundant
resident bird species in urban Singapore (per
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Tan 2016) with the number of urban
mortality records.
Spatial Distribution of Resident and
Migratory Building Collision Mortalities
To compare the spatial distribution
of resident and migratory building collision
mortalities, we filtered our dataset to
exclude records without complete GPS
coordinates and separately plotted resident
and migratory building collision mortality
records on a map of Singapore using QGIS
v2.18.9 (QGIS Development Team 2016).
For both the resident and migratory datasets,
we subsequently used the heatmap v0.2
plugin with a radius parameter set at 1,000
m and the QGIS raster calculator to identify
hotspots with a pixel value greater than two,
and overlaid the resident and migratory
collision hotspot polygons on a single map
canvas.
Results
Summary of Mortality Records
We documented a total of 362 mortality
records from 65 species during the surveyed
period, of which 104 mortalities were the
result of building collisions, 16 from
vehicular collisions, 10 due to predation – of
which 7 were attributable to cats – and 7
records resulting from misadventure (Table
1). 225 records had an unknown cause of
death, often due to specimens having been
moved post-mortem or specimens in
advanced stages of decay (Table 1). 21% (n
= 76) of the records were identified as
juveniles, with 24 building collision cases, 1
roadkill case, 1 instance of cat predation, 4
cases of misadventure, and 46 individuals
with an unknown cause of death (Table 1).
Pigeons (family Columbidae) formed
the largest proportion (32.6%) of the
mortality records, with 73 Pink-necked
Green Pigeon (Treron vernans) records
comprising 61.9% of the total pigeon
mortalities. Of the pigeon records with a
known cause of death, 88.9% were the result
of building collisions, which suggests that
pigeons may be especially susceptible to
collisions with urban structures.
Starlings and mynas (family
Sturnidae) were the second-largest taxon
amongst the reported urban mortalities
(22.1%), with most of the mortalities in this
family comprised of Asian Glossy Starlings
(Aplonis panayensis) and Javan Mynas
(Acridotheres javanicus). Interestingly,
juveniles formed 81% of the total Asian
Glossy Starling building collision records
(Fig. 1).
Plotting
the
distribution
of
mortalities over time, we find that juvenile
mortalities peak during the months of May
and June, and again in October and
November (Fig. 1). As for overall
mortalities, we observe a relative decrease in
the number of mortality records between the
months of May and September (Fig. 1).
Testing for Outliers
Correlating population densities with
number of mortalities for the 10 most
abundant species in Singapore, we find a
general positive linear correlation between
population density and number of
mortalities, with the exception of the Pinknecked Green Pigeons and Asian Glossy
Starlings, which exhibit far higher mortality
rates than would be expected based on their
population density (Fig. 2).
Comparing Resident and Migratory
Building Collisions
Plotting the spatial distribution of building
collision victims, we find two broad regions
where resident and migratory collision
hotspots overlap (Fig. 3), both of which are
located in the central region of Singapore
(see Low et al. (2017) for regional
delimitation of Singapore island), with one
hotspot occurring around the National
University of Singapore campus (Region A,
Fig. 3) and the other occurring over the
Heritage and Central Business Districts
(Region B, Fig. 3). We also observed an
absence of collision hotspots for resident
species in the western region of Singapore,
in contrast to the high number of migratory
building collisions in that region (Fig. 3;
Low et al. 2017).
Discussion
Our study documents for the first
time the wide array of non-migratory
Southeast Asian bird species affected by
anthropogenic sources of mortality, with
19
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
species representing all but one order
(podicipediformes) of resident avians known
for Singapore. However, it should be noted
that
our
opportunistic
sampling
methodology might result in artifacts that
may bias the data. Here we discuss the
implications of our data and the caveats that
need to be taken into account when
interpreting
our
dataset
for
each
anthropogenic mortality source.
Building Collisions
Our results show that while 32 nonmigratory species are affected by building
collisions (Table 1), some species are likely
more susceptible than others. In particular,
Pink-necked Green Pigeons and juvenile
Asian Glossy Starlings, and to a lesser
extent
the
Asian
Emerald
Doves
(Chalcophaps indica ), appear to be
overrepresented in the building collision
dataset (Table 1), and in the case of the
Pink-necked Green Pigeon and Asian
Glossy Starling, exhibit higher mortality
rates than their estimated population
densities would suggest (Fig. 2). The fact
that all three ‘super collider’ species are
forest-edge frugivores suggests that both
feeding guild and local dispersal behaviour
may affect a species’ susceptibility to
collision. Given the patchy distribution of
parks and forest fragments in Singapore
(Castelletta et al., 2005), it is likely that
these nomadic forest edge frugivores pass
through urban areas as part of their foraging
movements, which increases the likelihood
of building collisions occurring. Brisque et
al. (2017) have also found in Brazil that
Columbids appear to be more prone to
window collisions, which may explain why
all resident pigeon species in Singapore save
for the Rock Pigeon (Columba livia ) and the
extremely rare Little Green Pigeon (Treron
olax) are represented in our building
collision dataset (Lim, 2009). In addition,
the observation that juveniles form the
majority of Asian Glossy Starling building
collision mortalities suggests that collision
avoidance may be a learnt behaviour in this
species (Klem, 2014). It should be noted,
however, that sampling bias might also
contribute to the relatively high proportion
of Pink-necked Green Pigeon, Asian Glossy
20
Starling, and Asian Emerald Dove mortality
records. The large size and colourful
plumage of both pigeon species, as well as
the propensity for entire flocks of Asian
Glossy Starlings to collide with buildings at
the same time, result in these species being
highly conspicuous and detectable to casual
observers, and increases their likelihood of
being reported relative to other species
within
an
opportunistic
sampling
framework.
Comparing the number of resident
and migratory building collisions, our
results show that for the same sampling
period and the same sampling methodology,
we observe twice as many migratory
mortalities (n = 204) as resident mortalities
(n = 104; Table 1). This is consistent with
findings from both the neotropics and
nearctic, which show that migratory species
are more vulnerable to building collisions
than year-round residents (Agudelo-Álvarez
et al., 2010; Arnold and Zink, 2011; Kahle
et al., 2016).
As for the spatial distribution of
migratory and resident building collision
mortalities, while it is tempting to
overanalyse the results of the spatial
analysis, it should be noted that hotspots are
likely to be highly biased by uneven
sampling effort. The existence of
overlapping migratory and resident hotspots
over the National University of Singapore
(Region A, Fig. 3), for instance, is likely due
to a higher observer density relative to the
rest of Singapore. Regardless, the existence
of overlapping resident and migratory
hotspots in the Heritage and Central
Business District (Region B; Fig. 3) as well
as non-overlapping resident and migratory
hotspots in the central and western regions
of Singapore indicate that there are likely
both common and unique urban abiotic
factors affecting the likelihood of resident
and migratory building collision mortalities.
Roadkill and Cat Predation
In contrast to the building collision
mortalities, we observed far fewer roadkill
and cat predation mortalities in our dataset,
with twice as many roadkill mortalities as
cat predation mortalities (Table 1). The
results of our study appear to be incongruent
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
with the conclusions of Loss et al. (2013)
and Calvert et al. (2013), who find that cats
are responsible for the highest number of
avian mortalities in the United States and in
Canada respectively. This inconsistency
suggests that we have likely undersampled
the true extent of cat-based mortalities in our
study.
Temporal
variation
in
resident
mortalities
While the temporal pattern of
juvenile mortalities corresponds generally
with known breeding cycles in Singapore,
the observed dip in non-juvenile mortalities
in the middle of the year, with a slight
decline between May and June, and a larger
decline between July and September, does
not seem consistent with expectations since
adult mortality rates should remain
relatively stable throughout the year (Fig. 1).
The correlation of the non-juvenile mortality
peaks with the migratory months (October
to April) suggests that the mid-year dip
might
be
due
to
observational
autocorrelation, where observers are less
observant when overall mortalities are low
and vice versa, although this will need to be
ascertained using more structured sampling
methods.
Challenges and opportunities of citizen
science
The numerous caveats we have raised here
highlight the challenges of combining
opportunistic sampling with citizen science.
The uneven sampling of localities, varying
detectabilities of different species, and the
impacts of sampling autocorrelation and
sampling fatigue result in data that is often
inconsistent
and
incomplete,
which
confounds efforts at drawing rigorous
quantitative insights from the data. Despite
this, the results of our study show that
citizen science provides a cost-effective
means of gathering large amounts of data on
a diffuse and stochastic phenomenon, with
the added benefit of simultaneously
engaging in public outreach and education.
Our results therefore show that citizen
science can function as a cheap and effective
complement to more standardised survey
methodologies (Dickinson et al., 2010),
especially in intensively developed urban
areas such as Singapore.
Tables and Figures
Table 1: Summary of urban avian mortality records for Singapore, with families ordered per
Jarvis et al. (2014) and names following Eaton et al. (2016). Cause of death abbreviations are as
follows: BC, building collisions; RK, roadkill; CA, cat predation; PR, predation by unknown
predator; MA, misadventure; UK, unknown. Numbers in parentheses are numbers of juvenile
and fledgling mortalities.
Family
Anatidae
Species
Lesser Whistling-duck (Dendrocygna
Cause of Death
Total
BC
RK
CA
PR
MA
UK
-
-
-
-
-
1
1
javanica )
Phasianidae
Red Junglefowl (Gallus gallus)
1
1
-
-
-
2
4
Columbidae
Asian Emerald Dove (Chalcophaps
11
-
-
-
-
5
16
Rock Pigeon (Columba livia )
-
-
-
-
-
7
7
Pied Imperial Pigeon (Ducula bicolor )
2
1
-
-
-
1
4
Zebra Dove (Geopelia striata )
1
-
-
-
-
2
3
indica )
(1)
Spotted Dove (Spilopelia chinensis)
1
2
-
-
1
9
13
Pink-necked Green Pigeon (Treron
32
-
1
1
-
39
73
vernans)
(4)
(5)
21
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Thick-billed Green Pigeon (Treron
1
-
-
-
-
1
2
1
-
-
-
-
-
1
1
-
-
-
-
2
3
3
1
-
-
-
7
11
curvirostra )
Cuculidae
Banded Bay Cuckoo (Cacomantis
sonneratii)
Little Bronze Cuckoo (Chrysococcyx
minutillus)
Asian Koel (Eudynamys scolopaceus )
(1)
Caprimulgidae
(1)
Savanna Nightjar (Caprimulgus affinis )
-
-
-
-
-
1
1
Large-tailed Nightjar (Caprimulgus
-
-
-
-
-
4
4
1
-
-
-
-
3
4
Plume-toed Swiftlet (Colocalia affinis)
-
-
-
-
-
1
1
Grey-rumped Treeswift (Hemiprocne
-
-
-
-
-
1
1
-
4
1
-
-
3
8
Red-legged Crake (Rallina fasciata )
-
1
-
-
-
3
4
Slaty-breasted Rail (Lewinia striata )
-
-
-
-
-
3
3
Lapwing (Vanellus sp.)
-
-
-
-
-
1
1
macrurus)
Apodidae
Edible-nest Swiftlet (Aerodramus
fuciphagus)
Hemiprocnidae
longipennis)
Rallidae
White-breasted Waterhen (Amaurornis
phoenicurus)
Charadriidae
(1)
Ardeidae
Purple Heron (Ardea purpurea )
-
-
-
-
1
-
1
(1)
Accipitridae
Cattle Egret (Ardea ibis)
-
-
-
-
-
1
1
Striated Heron (Butorides striata )
-
-
-
-
-
3
3
Crested Goshawk (Lophospiza
2 (1)
-
-
-
-
2
4
trivirgata )
White-bellied Fish-eagle (Ichthyophaga
(1)
1
-
-
-
-
-
1
Brahminy Kite (Haliastur indus)
-
-
-
-
-
1
1
Changeable Hawk-Eagle (Nisaetus
2 (1)
-
-
-
-
-
2
Crested Serpent Eagle (Spilornis cheela )
1
-
-
-
-
-
1
Collared Scops Owl (Otus lempiji)
-
1
-
-
-
1
2
Spotted Wood Owl (Strix seloputo )
-
-
-
-
-
1
1
Barn Owl (Tyto alba )
1
-
-
-
-
3
4
Oriental Pied Hornbill (Anthracoceros
-
-
-
-
-
1
1
leucogaster )
limnaeetus)
Strigidae
Bucerotidae
albirostris)
Megalaimidae
Coppersmith Barbet (Psilopogon
(1)
1
-
-
-
-
3
4
Lineated Barbet (Psilopogon lineatus)
1
-
-
-
-
-
1
Sunda Pygmy-woodpecker (Picoides
-
-
-
-
-
1
1
haemacephalus)
Picidae
moluccensis)
22
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
Common Flameback (Dinopium
-
-
-
-
javanense)
Alcedinidae
White-breasted Kingfisher (Halcyon
1
1
3
4
(1)
1
-
-
-
-
smyrnensis)
Collared Kingfisher (Todiramphus
-
(1)
1
-
-
-
-
2
3
-
-
-
-
-
1
1
chloris)
Coraciidae
Common Dollarbird (Eurystomus
orientalis)
Psittacidae
Blue-crowned Hanging Parrot (Loriculus
(1)
1
-
-
-
-
1
2
1
-
-
-
-
1
2
1
-
-
-
-
1
2
galgulus)
Red-breasted Parakeet (Psittacula
alexandri)
Long-tailed Parakeet (Psittacula
longicauda )
(1)
Aegithinidae
Common Iora (Aegithina tiphia )
-
-
-
-
-
2
2
Cisticolidae
Ashy Tailorbird (Orthotomus ruficeps )
-
-
-
-
-
1
1
Common Tailorbird (Orthotomus
-
-
-
-
1
-
1
sutorius)
Dicaedae
Scarlet-backed Flowerpecker (Dicaeum
(1)
3 (1)
-
-
-
-
2
5
-
-
-
1
-
1
2
White-headed Munia (Lonchura maja )
1
-
-
-
-
-
1
Scaly-breasted Munia (Lonchura
2
-
-
-
-
5
7
Javan Munia (Lonchura leucogastroides )
-
-
-
-
-
1
1
Irenidae
Asian Fairy Bluebird (Irena puella )
-
-
-
-
-
1
1
Muscicapidae
Oriental Magpie-robin (Copsychus
1
-
1
-
-
3
5
cruentatum)
Dicruridae
Greater Racket-tailed Drongo (Dicrurus
paradiseus)
Estrildidae
punctulata )
saularis)
Nectariniidae
Brown-throated Sunbird (Anthreptes
(2)
-
-
-
-
-
malacensis)
Ornate Sunbird (Cinnyris ornatus)
1
(1)
-
-
1
-
-
(1)
Little Spiderhunter (Arachnothera
1
3
4
(1)
-
-
-
-
-
1
1
-
2
1
-
1
6
10
(1)
(4)
-
2
longirostra )
Oriolidae
Passeridae
Black-naped Oriole (Oriolus chinensis)
Eurasian Tree Sparrow (Passer
2
-
1
-
montanus)
Pycnonotidae
Sunda Yellow-vented Bulbul
(1)
-
-
-
-
-
(Pycnonotus analis)
Olive-winged Bulbul (Pyccnonotus
5
16
16
(5)
2
-
-
-
-
1
3
2
3
-
1
2
22
30
plumosus)
Sturnidae
Javan Myna (Actidotheres javanicus)
23
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
(5)
Zosteropidae
Common Myna (Acridotheres tristis)
-
-
-
-
-
1
1
Asian Glossy Starling (Aplonis
21
-
-
-
-
26
47
panayensis)
(17)
Common Hill Myna (Gracula religiosa )
-
-
-
-
-
2
2
Sunda White-eye (Zosterops melanurus)
1
-
1
-
-
6
8
(13)
(1)
Total
104
16
7
3
7
225
362
Figure 1: Reported resident mortalities by month, stratified by age category. The two peaks in
juvenile and fledgling mortalities in May and November likely correspond with primary and
secondary breeding periods (Lim, 2009). It is unclear why there exists a dip in mortality records
during the months of July to September.
Correla on between avian popula on density and number
of mortali es for the 10 most abundant bird species
80
Pink-necked Green
Pigeon
70
Numner of Mortali es
60
50
Asian Glossy Starling
40
y = 14.649x
R² = -0.5047
30
20
10
0
0
0.5
1
1.5
2
2.5
3
Popula on Density (ha-1)
Figure 2: Correlation between avian population density (derived from Tan (2016)) and number
of mortalities for the 10 most abundant species in Singapore. The scatterplot shows a general
positive linear correlation between population density and number of recorded mortalities, with
24
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
the notable exception of the Pink-necked Green Pigeon and the Asian Glossy Starling, which
suggests that these two species may either be more susceptible to urban mortalities or subject to
positive sampling bias.
Figure 3: Spatial distribution of resident and migratory building collisions in Singapore, with
shaded regions highlighting likely collision hotspots. Overlaying the inferred collision hotspots
of both resident and migratory species shows two regions of overlap, with one region centering
around the National University of Singapore campus (region A) and the other around the
Heritage and Central Business Districts (region B)
Mortality in Canada. Avian Conserv.
Ecol.
8,
11.
References
Agudelo-Álvarez, L., Moreno-Velasquez, J.,
https://doi.org/http://dx.doi.org/10.5751
Ocampo-Peñuela, N., 2010. Colisiones
/ACE-00581-080211
de aves contra ventanales en un campus
Castelletta, M., Thiollay, J.-M., Sodhi, N.S.,
universitario de bogotá, colombia.
2005. The effects of extreme forest
Ornitol. Colomb. 10, 3–10.
fragmentation on the bird community
Arnold, T.W., Zink, R.M., 2011. Collision
of Singapore Island. Biol. Conserv.
mortality has no discernible effect on
121,
135–155.
population trends of North American
https://doi.org/10.1016/j.biocon.2004.0
birds.
PLoS
One
6,
1–6.
3.033
https://doi.org/10.1371/journal.pone.00
Chan, L., Hillel, O., Elmqvist, T., Werner,
24708
P., Holman, N., Mader, A., Calcaterra,
Brisque, T., Campos-Silva, L.A., Piratelli,
E., 2014. USER ’ S MANUAL ON
A.J., 2017. Relationship between birdTHE SINGAPORE INDEX ON
of-prey decals and bird-window
CITIES ’ BIODIVERSITY ( also
collisions on a Brazilian university
known as the City Biodiversity Index ).
campus.
Zoologia
34,
1–8.
National Parks Board, Singapore,
https://doi.org/10.3897/zoologia.34.e13
Singapore.
729
Dickinson, J.L., Zuckerberg, B., Bonter,
Calvert, A.M., Bishop, C. a, Elliot, R.D.,
D.N., 2010. Citizen Science as an
Krebs, E. a, Kydd, T.M., Machtans,
Ecological Research Tool: Challenges
C.S., Robertson, G.J., 2013. A
and Benefits. Annu. Rev. Ecol. Evol.
Synthesis of Human-related Avian
Syst.
41,
149–172.
25
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
https://doi.org/10.1146/annurevecolsys-102209-144636
Eaton, J.A., van Balen, B., Brickle, N.W.,
Rheindt, F.E., 2016. Birds of the
Indonesian
Archipelago:
Greater
Sundas and Wallacea, First. ed. Lynx
Edicions, Barcelona.
Feng, Z., 2013. Team flocks to collect dead
birds for research. The Straits Times.
Jarvis, E.D., Mirarab, S., Aberer, A.J., Li,
B., Houde, P., Li, C., Ho, S.Y.W.,
Faircloth, B.C., Nabholz, B., Howard,
J.T., Suh, A., Weber, C.C., da Fonseca,
R.R., Li, J., Zhang, F., Li, H., Zhou, L.,
Narula, N., Liu, L., Ganapathy, G.,
Boussau,
B.,
Bayzid,
M.S.,
Zavidovych, V., Subramanian, S.,
Gabaldon, T., Capella-Gutierrez, S.,
Huerta-Cepas, J., Rekepalli, B., Munch,
K., Schierup, M., Lindow, B., Warren,
W.C., Ray, D., Green, R.E., Bruford,
M.W., Zhan, X., Dixon, A., Li, S., Li,
N., Huang, Y., Derryberry, E.P.,
Bertelsen, M.F., Sheldon, F.H.,
Brumfield, R.T., Mello, C. V., Lovell,
P. V., Wirthlin, M., Schneider, M.P.C.,
Prosdocimi, F., Samaniego, J.A.,
Velazquez, A.M. V., Alfaro-Nunez, A.,
Campos, P.F., Petersen, B., SicheritzPonten, T., Pas, A., Bailey, T.,
Scofield, P., Bunce, M., Lambert,
D.M., Zhou, Q., Perelman, P., Driskell,
A.C., Shapiro, B., Xiong, Z., Zeng, Y.,
Liu, S., Li, Z., Liu, B., Wu, K., Xiao,
J., Yinqi, X., Zheng, Q., Zhang, Y.,
Yang, H., Wang, J., Smeds, L.,
Rheindt, F.E., Braun, M., Fjeldsa, J.,
Orlando, L., Barker, F.K., Jonsson,
K.A., Johnson, W., Koepfli, K.-P.,
O’Brien, S., Haussler, D., Ryder, O.A.,
Rahbek, C., Willerslev, E., Graves,
G.R., Glenn, T.C., McCormack, J.,
Burt, D., Ellegren, H., Alstrom, P.,
Edwards, S. V., Stamatakis, A.,
Mindell, D.P., Cracraft, J., Braun, E.L.,
Warnow, T., Jun, W., Gilbert, M.T.P.,
Zhang, G., 2014. Whole-genome
analyses resolve early branches in the
tree of life of modern birds. Science
(80-.
).
346,
1320–1331.
https://doi.org/10.1126/science.125345
1
Kahle, L.Q., Flannery, M.E., Dumbacher,
26
J.P., 2016. Bird-Window Collisions at a
West-Coast Urban Park Museum:
Analyses of Bird Biology and Window
Attributes from Golden Gate Park, San
Francisco. PLoS One 11, e0144600.
https://doi.org/10.1371/journal.pone.01
44600
Klem, D., 2015. Bird-Window Collisions: A
Critical
Animal
Welfare
and
Conservation Issue. Appl. Anim. Welf.
Sci.
18,
S11–S17.
https://doi.org/10.1080/10888705.2015.
1075832
Klem, D., 2014. Landscape, Legal, and
Biodiversity Threats that Windows
Pose to Birds: A Review of an
Important Conservation Issue. Land 3,
351–361.
https://doi.org/10.3390/land3010351
Klem, D., 1989. Bird-window collisions.
Wilson Bull. 4, 606–620.
Kociolek, A. V., Clevenger, A.P., St. Clair,
C.C., Proppe, D.S., 2011. Effects of
Road Networks on Bird Populations.
Conserv.
Biol.
25,
241–249.
https://doi.org/10.1111/j.15231739.2010.01635.x
Lepczyk, C.A., Mertig, A.G., Liu, J., 2004.
Landowners and cat predation across
rural-to-urban
landscapes.
Biol.
Conserv.
115,
191–201.
https://doi.org/10.1016/S00063207(03)00107-1
Lim, K.S., 2009. The Avifauna of
Singapore. Nature Society (Singapore),
Singapore.
Loss, S.R., Will, T., Loss, S.S., Marra, P.P.,
2014. Bird–building collisions in the
United States: Estimates of annual
mortality and species vulnerability.
Condor
116,
8–23.
https://doi.org/10.1650/CONDOR-13090.1
Loss, S.R., Will, T., Marra, P.P., 2015.
Direct Mortality of Birds from
Anthropogenic Causes. Annu. Rev.
Ecol. Evol. Syst. 46, 99–120.
https://doi.org/10.1146/annurevecolsys-112414-054133
Loss, S.R., Will, T., Marra, P.P., 2013. The
impact of free-ranging domestic cats on
wildlife of the United States. Nat.
Commun.
4,
1396.
David J. X. TAN,
et al. (2017) Int. J. Trop. Vet. Biomed. Res.2:17-23
https://doi.org/10.1038/ncomms2380
Low, B.W., Yong, D.L., Tan, D., Owyong,
A., Chia, A., 2017. Migratory bird
collisions with man-made structures in
South-East Asia : a case study from
Singapore. BirdingASIA 27, 107–111.
Tan, D.J.X., 2016. A quantitative survey of
avian population densities in a
heterogeneous
tropical
urban
landscape. Raffles Bull. Zool. 2016.
Tan, D.J.X., 2015. Population Dynamics of
the Striped Tit-Babbler in Singapore.
National University of Singapore.
United Nations, Department of Economic
and Social Affairs, P.D., 2015. World
urbanization prospects. United Nations,
New York.
Woinarski, J.C.Z., Murphy, B.P., Legge,
S.M., Garnett, S.T., Lawes, M.J.,
Comer, S., Dickman, C.R., Doherty,
T.S., Edwards, G., Nankivell, A.,
Paton, D., Palmer, R., Woolley, L.A.,
2017. How many birds are killed by
cats in Australia? Biol. Conserv. 214,
76–87.
https://doi.org/10.1016/j.biocon.2017.0
8.006
Yee, A.T.K., Corlett, R.T., Liew, S.C., Tan,
H.T.W., 2011. The vegetation of
Singapore ― an updated map. Gard.
Bull. Singapore 63, 205–212.
27